Seasonality and chemical elicitation of defense oleoresin production in field-grown slash pine under subtropical climate

Rodrigues-Corrêa, Kelly Cristine da Silva; Fett-Neto, Arthur Germano

Abstract

Oleoresin is a key defense strategy of advanced gymnosperms, based on the combination of a complex anatomical structure of resin ducts and elaborate terpene biochemistry. Given the vast array of oleoresin economic applications in the chemical, pharmaceutical, agrochemical, and biofuel industries, translating factors that regulate terpene biosynthesis into higher oleoresin yield is a challenge for the forestry industry. Field tests with approximately 3,500 28-year-old slash pine (Pinus elliottii Engelm. var. elliottii) trees were carried out from 2005 to 2008, under the subtropical climate of Southern Brazil, in order to examine the seasonal profile of oleoresin production stimulation in response to different chemical adjuvants, after mechanical injury. Yields of trees treated with oleoresin-inducing pastes containing alternative adjuvants were compared to the standard commercial one used on an industrial scale (based on the ethylene-releasing compound - 2-chloroethylphosphonic acid - CEPA). Significant increases in pine oleoresin yield were observed by modulating its biosynthesis and using chemical stimulants affecting defense responses (benzoic acid, used in addition to CEPA) and biosynthetic enzymes (metal cofactors of terpene synthases, iron or potassium, used as replacements for CEPA). Oleoresin stimulation was consistent over at least four consecutive years. Overall effectiveness of oleoresin yield adjuvant stimulation was higher in the faster growth seasons, although potassium was effective in all of them. Combining metal cofactors did not show synergistic or additive interactions. The results suggest that higher oleoresin yields can be obtained by using individual adjuvants of the same signaling pathway in a season-specific fashion.

mechanical wounding; benzoic acid; metal cofactors; potassium; iron; terpene synthases; resin tapping

Aaltonen H, Pumpanen J, Pihlatie M, Hakola H, Hellen H, Kulmala L, et al (2011) Boreal pine forest floor biogenic volatile organic compound emissions peak in early summer and autumn. Agricultural and Forest Meteorology 151:682-691.
Brito JO, Barrichelo LEG, Gutierrez LE, Trevisan JF (1978) Resina de Pinus implantados no Brasil: resinagem e qualidade de resinas de pinheiros tropicais: comparações entre espécies e época de resinagem. Instituto de Pesquisas e Estudos Florestais; ESALQ-USP, Circular técnica 35.
Cunningham A (2012) Pine resin tapping techniques. In: Fett-Neto AG, Rodrigues-Corrêa KCS (eds), Pine resin: biology, chemistry and applications, pp. 1-8. Research Signpost, Kerala, India.
Fäldt J, Martin D, Miller B, Rawat S, Bohlmann J (2003) Traumatic resin defense in Norway spruce (Picea abies): methyl jasmonate-induced terpene synthase gene expression, and cDNA cloning and functional characterization of (+)-3-carene synthase. Plant Molecular Biology 51:119-133.
Ferreira AG, Fior CS, Gualtieri SCJ (2011) Oleoresin yield of Pinus elliottii Engelm. seedlings. Brazilian Journal of Plant Physiology 23:313-316.
Figueiredo-Filho A, Machado SA, Hosokawa RT, Kikute P (1992) Avaliação econômica da resinagem em floresta de Pinus elliottii Engelm. var. elliottii Instituto de Pesquisas e Estudos Florestais, Circular Técnica 45:48-63.
Hall DE, Zerbe P, Jancsik S, Quesada AL, Dullat H, Madilao LL, et al (2013) Evolution of conifer diterpene synthases: diterpene resin acid biosynthesis in Lodgepole Pine and Jack Pine involves monofunctional and bifunctional diterpene synthases. Plant Physiology 161:600-616.
Hodges JD, Elam WW, Bluhm DR (1981) Influence of resin duct size and number on oleoresin flow in the southern pines. USDA Forest Service Research Note SO-266, Southern Forest Experiment Station, New Orleans.
Holzke C, Hoffmann T, Jaeger L, Koppmann R, Zimmer W (2006) Diurnal and seasonal variation of monoterpene and sesquiterpene emissions from Scots pine (Pinus sylvestris L.). Atmospheric Environment 40:3174-3185.
Huber DPW, Ralph S, Bohlmann J (2004) Genomic hardwiring and phenotypic plasticity of terpenoid-based defenses in conifers. Journal of Chemical Ecology 30:2399-2418.
Hudgins JW, Franceschi VR (2004) Methyl jasmonate-induced ethylene production is responsible for conifer phloem defense responses and reprogramming of stem cambial zone for traumatic resin duct formation. Plant Physiology 135:2134-2149.
Keeling CI, Bohlmann J (2006) Diterpene resin acids in conifers. Phytochemistry 67:2415-2423.
Kim JC, Kim KJ, Kim DS, Han JS (2005) Seasonal variations of monoterpene emissions from coniferous trees of different ages in Korea. Chemosphere 59:1685-1696.
Krajnc AU, Kristl J, Ivancic A (2011) Application of salicylic acid induces antioxidant defense responses in the phloem of Picea abies and inhibits colonization by Ips typographus Forest Ecology and Management 261:416-426.
Lewinsohn E, Gijzen M, Muzika RM, Barton K, Croteau R (1993) Oleoresinosis in Grand Fir (Abies grandis) saplings and mature trees (Modulation of this wound response by light and water stresses). Plant Physiology 101:1021-1028.
Lim JH, Kim JC, Kim KJ, Son YS, Sunwoo Y, Han JS (2008) Seasonal variations of monoterpene emissions from Pinus densiflora in East Asia. Chemosphere 73:470-478.
Lombardero MJ, Ayres MP, Ayres BD (2006) Effects of fire and mechanical wounding on Pinus resinosa resin defenses, beetle attacks, and pathogens. Forest Ecology and Management 225:349-358.
McKay SAB, Godard KA, Toudefallah M, Martin DM, Alfaro R, King J, et al (2006) Wound-induced terpene synthase gene expression in Sitka spruce that exhibit resistance or susceptibility to attack by the white pine weevil. Plant Physiology 140:1009-1021.
McKay SAB, Hunter WL, Godard KA, Wang SX, Martin DM, Bohlmann J, et al (2003) Insect attack and wounding induce traumatic resin duct development and gene expression of (-)-Pinene Synthase in Sitka spruce. Plant Physiology 133:600-616.
Peñuelas J, Llusià J (1999) Short-term responses of terpene emission rates to experimental changes of PFD in Pinus halepensis and Quercus ilex in summer field conditions. Environmental and Experimental Botany 42:61-68.
Phillips M (2012) Inducible and constitutive defenses in pine: the ecological role of pine oil. In: Fett-Neto AG, Rodrigues-Corrêa KCS (eds), Pine resin: biology, chemistry and applications, pp. 49-66. Research Signpost, Kerala, India.
Pio CA, Valente AA (1998) Atmospheric fluxes and concentrations of monoterpenes in resin-tapped pine forests. Atmospheric Environment 32:683-691.
Räisänen T, Ryyppö A, Kellomäki S (2009) Monoterpene emission of a boreal Scots pine (Pinus sylvestris L.) forest. Agricultural and Forest Meteorology 149:808-819.
Rigling A, Bruhlhart H, Braker OU, Forster T, Schweingruber FH (2003) Effects of irrigation on diameter growth and vertical resin duct production in Pinus sylvestris L. on dry sites in the central Alps, Switzerland. Forest Ecology and Management 175:285-296.
Rodrigues-Corrêa KCS, Fett-Neto AG (2012) Physiological control of pine resin production. In: Fett-Neto AG, Rodrigues-Corrêa KCS (eds), Pine resin: biology, chemistry and applications, pp. 25-48. Research Signpost, Kerala, India.
Rodrigues-Corrêa KCS, de Lima JC, Fett-Neto AG (2012) Pine oleoresin: tapping green chemicals, biofuels, food protection, and carbon sequestration from multipurpose trees. Food and Energy Security 1:81-93.
Rodrigues KCS, Apel MA, Henriques AT, Fett-Neto AG (2011) Efficient oleoresin biomass production in pines using low cost metal containing stimulant paste. Biomass and Bioenergy 35:4442-4448.
Rodrigues KCS, Azevedo PCN, Sobreiro LE, Pelissari P, Fett AG (2008) Oleoresin yield of Pinus elliottii plantations in a subtropical climate: Effect of tree diameter, wound shape and concentration of active adjuvants in resin stimulating paste. Industrial Crops and Products 27:322-327.
Rodrigues KCS, Fett-Neto AG (2009) Oleoresin yield of Pinus elliottii in a subtropical climate: Seasonal variation and effect of auxin and salicylic acid-based stimulant paste. Industrial Crops and Products 30:316-320.
Rodriguez FI, Esch JJ, Hall AE, Binder BM, Schaller GE, Bleecker AB (1999) A copper cofactor for the ethylene receptor ETR1 from Arabidopsis Science 283:996-998.
Savage TJ, Hatch MW, Croteau R (1994) Monoterpene synthases of Pinus contorta and related conifers. A new class of terpenoid cyclase. Journal of Biological Chemistry 269:4012-4020.
Schmidt A, Nagel R, Krekling T, Christiansen E, Gershenzon J, Krokene P (2011) Induction of isoprenyl diphosphate synthases, plant hormones and defense signalling genes correlates with traumatic resin duct formation in Norway spruce (Picea abies). Plant Molecular Biology 77:577-590.
Shah J (2003) The salicylic acid loop in plant defense. Current Opinion in Plant Biology 6:365-371.
Tingey DT, Manning M, Grothaus LC, Burns WF (1980) Influence of light and temperature on monoterpene emission rates from slash pine. Plant Physiology 65:797-801.
Tisdale RA, Nebeker TE, Hodges JD (2003) The role of oleoresin flow in the induced response of loblolly pine to a southern pine beetle associated fungus. Canadian Journal of Botany 81:368-374.

Publication Dates

Publication in this collection
02 July 2015
Date of issue
2013

History

Received
17 Apr 2013
Accepted
30 Apr 2013

This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.

[1] Aaltonen H, Pumpanen J, Pihlatie M, Hakola H, Hellen H, Kulmala L, et al (2011) Boreal pine forest floor biogenic volatile organic compound emissions peak in early summer and autumn. Agricultural and Forest Meteorology 151:682-691.

[2] Brito JO, Barrichelo LEG, Gutierrez LE, Trevisan JF (1978) Resina de Pinus implantados no Brasil: resinagem e qualidade de resinas de pinheiros tropicais: comparações entre espécies e época de resinagem. Instituto de Pesquisas e Estudos Florestais; ESALQ-USP, Circular técnica 35.

[3] Cunningham A (2012) Pine resin tapping techniques. In: Fett-Neto AG, Rodrigues-Corrêa KCS (eds), Pine resin: biology, chemistry and applications, pp. 1-8. Research Signpost, Kerala, India.

[4] Fäldt J, Martin D, Miller B, Rawat S, Bohlmann J (2003) Traumatic resin defense in Norway spruce (Picea abies): methyl jasmonate-induced terpene synthase gene expression, and cDNA cloning and functional characterization of (+)-3-carene synthase. Plant Molecular Biology 51:119-133.

[5] Ferreira AG, Fior CS, Gualtieri SCJ (2011) Oleoresin yield of Pinus elliottii Engelm. seedlings. Brazilian Journal of Plant Physiology 23:313-316.

[6] Figueiredo-Filho A, Machado SA, Hosokawa RT, Kikute P (1992) Avaliação econômica da resinagem em floresta de Pinus elliottii Engelm. var. elliottii Instituto de Pesquisas e Estudos Florestais, Circular Técnica 45:48-63.

[7] Hall DE, Zerbe P, Jancsik S, Quesada AL, Dullat H, Madilao LL, et al (2013) Evolution of conifer diterpene synthases: diterpene resin acid biosynthesis in Lodgepole Pine and Jack Pine involves monofunctional and bifunctional diterpene synthases. Plant Physiology 161:600-616.

[8] Hodges JD, Elam WW, Bluhm DR (1981) Influence of resin duct size and number on oleoresin flow in the southern pines. USDA Forest Service Research Note SO-266, Southern Forest Experiment Station, New Orleans.

[9] Holzke C, Hoffmann T, Jaeger L, Koppmann R, Zimmer W (2006) Diurnal and seasonal variation of monoterpene and sesquiterpene emissions from Scots pine (Pinus sylvestris L.). Atmospheric Environment 40:3174-3185.

[10] Huber DPW, Ralph S, Bohlmann J (2004) Genomic hardwiring and phenotypic plasticity of terpenoid-based defenses in conifers. Journal of Chemical Ecology 30:2399-2418.

[11] Hudgins JW, Franceschi VR (2004) Methyl jasmonate-induced ethylene production is responsible for conifer phloem defense responses and reprogramming of stem cambial zone for traumatic resin duct formation. Plant Physiology 135:2134-2149.

[12] Keeling CI, Bohlmann J (2006) Diterpene resin acids in conifers. Phytochemistry 67:2415-2423.

[13] Kim JC, Kim KJ, Kim DS, Han JS (2005) Seasonal variations of monoterpene emissions from coniferous trees of different ages in Korea. Chemosphere 59:1685-1696.

[14] Krajnc AU, Kristl J, Ivancic A (2011) Application of salicylic acid induces antioxidant defense responses in the phloem of Picea abies and inhibits colonization by Ips typographus Forest Ecology and Management 261:416-426.

[15] Lewinsohn E, Gijzen M, Muzika RM, Barton K, Croteau R (1993) Oleoresinosis in Grand Fir (Abies grandis) saplings and mature trees (Modulation of this wound response by light and water stresses). Plant Physiology 101:1021-1028.

[16] Lim JH, Kim JC, Kim KJ, Son YS, Sunwoo Y, Han JS (2008) Seasonal variations of monoterpene emissions from Pinus densiflora in East Asia. Chemosphere 73:470-478.

[17] Lombardero MJ, Ayres MP, Ayres BD (2006) Effects of fire and mechanical wounding on Pinus resinosa resin defenses, beetle attacks, and pathogens. Forest Ecology and Management 225:349-358.

[18] McKay SAB, Godard KA, Toudefallah M, Martin DM, Alfaro R, King J, et al (2006) Wound-induced terpene synthase gene expression in Sitka spruce that exhibit resistance or susceptibility to attack by the white pine weevil. Plant Physiology 140:1009-1021.

[19] McKay SAB, Hunter WL, Godard KA, Wang SX, Martin DM, Bohlmann J, et al (2003) Insect attack and wounding induce traumatic resin duct development and gene expression of (-)-Pinene Synthase in Sitka spruce. Plant Physiology 133:600-616.

[20] Peñuelas J, Llusià J (1999) Short-term responses of terpene emission rates to experimental changes of PFD in Pinus halepensis and Quercus ilex in summer field conditions. Environmental and Experimental Botany 42:61-68.

[21] Phillips M (2012) Inducible and constitutive defenses in pine: the ecological role of pine oil. In: Fett-Neto AG, Rodrigues-Corrêa KCS (eds), Pine resin: biology, chemistry and applications, pp. 49-66. Research Signpost, Kerala, India.

[22] Pio CA, Valente AA (1998) Atmospheric fluxes and concentrations of monoterpenes in resin-tapped pine forests. Atmospheric Environment 32:683-691.

[23] Räisänen T, Ryyppö A, Kellomäki S (2009) Monoterpene emission of a boreal Scots pine (Pinus sylvestris L.) forest. Agricultural and Forest Meteorology 149:808-819.

[24] Rigling A, Bruhlhart H, Braker OU, Forster T, Schweingruber FH (2003) Effects of irrigation on diameter growth and vertical resin duct production in Pinus sylvestris L. on dry sites in the central Alps, Switzerland. Forest Ecology and Management 175:285-296.

[25] Rodrigues-Corrêa KCS, Fett-Neto AG (2012) Physiological control of pine resin production. In: Fett-Neto AG, Rodrigues-Corrêa KCS (eds), Pine resin: biology, chemistry and applications, pp. 25-48. Research Signpost, Kerala, India.

[26] Rodrigues-Corrêa KCS, de Lima JC, Fett-Neto AG (2012) Pine oleoresin: tapping green chemicals, biofuels, food protection, and carbon sequestration from multipurpose trees. Food and Energy Security 1:81-93.

[27] Rodrigues KCS, Apel MA, Henriques AT, Fett-Neto AG (2011) Efficient oleoresin biomass production in pines using low cost metal containing stimulant paste. Biomass and Bioenergy 35:4442-4448.

[28] Rodrigues KCS, Azevedo PCN, Sobreiro LE, Pelissari P, Fett AG (2008) Oleoresin yield of Pinus elliottii plantations in a subtropical climate: Effect of tree diameter, wound shape and concentration of active adjuvants in resin stimulating paste. Industrial Crops and Products 27:322-327.

[29] Rodrigues KCS, Fett-Neto AG (2009) Oleoresin yield of Pinus elliottii in a subtropical climate: Seasonal variation and effect of auxin and salicylic acid-based stimulant paste. Industrial Crops and Products 30:316-320.

[30] Rodriguez FI, Esch JJ, Hall AE, Binder BM, Schaller GE, Bleecker AB (1999) A copper cofactor for the ethylene receptor ETR1 from Arabidopsis Science 283:996-998.

[31] Savage TJ, Hatch MW, Croteau R (1994) Monoterpene synthases of Pinus contorta and related conifers. A new class of terpenoid cyclase. Journal of Biological Chemistry 269:4012-4020.

[32] Schmidt A, Nagel R, Krekling T, Christiansen E, Gershenzon J, Krokene P (2011) Induction of isoprenyl diphosphate synthases, plant hormones and defense signalling genes correlates with traumatic resin duct formation in Norway spruce (Picea abies). Plant Molecular Biology 77:577-590.

[33] Shah J (2003) The salicylic acid loop in plant defense. Current Opinion in Plant Biology 6:365-371.

[34] Tingey DT, Manning M, Grothaus LC, Burns WF (1980) Influence of light and temperature on monoterpene emission rates from slash pine. Plant Physiology 65:797-801.

[35] Tisdale RA, Nebeker TE, Hodges JD (2003) The role of oleoresin flow in the induced response of loblolly pine to a southern pine beetle associated fungus. Canadian Journal of Botany 81:368-374.

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Seasonality and chemical elicitation of defense oleoresin production in field-grown slash pine under subtropical climate

Abstract

Publication Dates

History